TY - JOUR
T1 - The AMOR Arabinogalactan Sugar Chain Induces Pollen-Tube Competency to Respond to Ovular Guidance
AU - Mizukami, Akane G.
AU - Inatsugi, Rie
AU - Jiao, Jiao
AU - Kotake, Toshihisa
AU - Kuwata, Keiko
AU - Ootani, Kento
AU - Okuda, Satohiro
AU - Sankaranarayanan, Subramanian
AU - Sato, Yoshikatsu
AU - Maruyama, Daisuke
AU - Iwai, Hiroaki
AU - Garénaux, Estelle
AU - Sato, Chihiro
AU - Kitajima, Ken
AU - Tsumuraya, Yoichi
AU - Mori, Hitoshi
AU - Yamaguchi, Junichiro
AU - Itami, Kenichiro
AU - Sasaki, Narie
AU - Higashiyama, Tetsuya
N1 - Funding Information:
We thank Y. Amagai, Y. Yano, and S. Sakamoto, undergraduate students of the University of Tokyo and Nagoya University, for their assistance in preparing medium for large-scale ovule and ovary culture. We also thank M.M. Kanaoka, T. Kuroiwa, T. Ueda, and A. Nakano for helpful comments; H. Takeuchi for critical reading of the manuscript; M. Kuzuya and R. Yui for help with biochemical analysis; K. Ogasawara and A. Terashima for help with frozen sectioning of Torenia pistils; K. Takahashi for help with LC-MS analysis; N. Kamiya for help with LURE bead assays; and D. Kurihara, Y. Hamamura, and S. Nagahara for their assistance with time-lapse imaging. A.G.M. and S.O. were supported by grants 7802 and 30004 , respectively, from the Japan Society for the Promotion of Science Fellowships. This work was supported in part by grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan ( 17027006 , 17657022 , 18075004 , and 19370017 to T.H.), Program for the Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN to T.H.), Yamada Science Foundation (to T.H.), Mitsubishi Foundation (to T.H.), Japan Advanced Plant Science Network , and Japan Science and Technology Agency (CREST, PRESTO, and ERATO projects to T.H.).
Publisher Copyright:
© 2016 Elsevier Ltd. All rights reserved.
PY - 2016/4/25
Y1 - 2016/4/25
N2 - Precise directional control of pollen-tube growth by pistil tissue is critical for successful fertilization of flowering plants [1-3]. Ovular attractant peptides, which are secreted from two synergid cells on the side of the egg cell, have been identified [4-6]. Emerging evidence suggests that the ovular directional cue is not sufficient for successful guidance but that competency control by the pistil is critical for the response of pollen tubes to the attraction signal [1, 3, 7]. However, the female molecule for this competency induction has not been reported. Here we report that ovular methyl-glucuronosyl arabinogalactan (AMOR) induces competency of the pollen tube to respond to ovular attractant LURE peptides in Torenia fournieri. We developed a method for assaying the response capability of a pollen tube by micromanipulating an ovule. Using this method, we showed that pollen tubes growing through a cut style acquired a response capability in the medium by receiving a sufficient amount of a factor derived from mature ovules of Torenia. This factor, named AMOR, was identified as an arabinogalactan polysaccharide, the terminal 4-O-methyl-glucuronosyl residue of which was necessary for its activity. Moreover, a chemically synthesized disaccharide, the β isomer of methyl-glucuronosyl galactose (4-Me-GlcA-β-(1→6)-Gal), showed AMOR activity. No specific sugar-chain structure of plant extracellular matrix has been identified as a bioactive molecule involved in intercellular communication. We suggest that the AMOR sugar chain in the ovary renders the pollen tube competent to the chemotropic response prior to final guidance by LURE peptides.
AB - Precise directional control of pollen-tube growth by pistil tissue is critical for successful fertilization of flowering plants [1-3]. Ovular attractant peptides, which are secreted from two synergid cells on the side of the egg cell, have been identified [4-6]. Emerging evidence suggests that the ovular directional cue is not sufficient for successful guidance but that competency control by the pistil is critical for the response of pollen tubes to the attraction signal [1, 3, 7]. However, the female molecule for this competency induction has not been reported. Here we report that ovular methyl-glucuronosyl arabinogalactan (AMOR) induces competency of the pollen tube to respond to ovular attractant LURE peptides in Torenia fournieri. We developed a method for assaying the response capability of a pollen tube by micromanipulating an ovule. Using this method, we showed that pollen tubes growing through a cut style acquired a response capability in the medium by receiving a sufficient amount of a factor derived from mature ovules of Torenia. This factor, named AMOR, was identified as an arabinogalactan polysaccharide, the terminal 4-O-methyl-glucuronosyl residue of which was necessary for its activity. Moreover, a chemically synthesized disaccharide, the β isomer of methyl-glucuronosyl galactose (4-Me-GlcA-β-(1→6)-Gal), showed AMOR activity. No specific sugar-chain structure of plant extracellular matrix has been identified as a bioactive molecule involved in intercellular communication. We suggest that the AMOR sugar chain in the ovary renders the pollen tube competent to the chemotropic response prior to final guidance by LURE peptides.
KW - LURE attractant peptides
KW - Torenia
KW - arabinogalactan
KW - competency control
KW - ovule
KW - pollen-tube guidance
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UR - http://www.scopus.com/inward/citedby.url?scp=84962676184&partnerID=8YFLogxK
U2 - 10.1016/j.cub.2016.02.040
DO - 10.1016/j.cub.2016.02.040
M3 - Article
C2 - 27068416
AN - SCOPUS:84962676184
SN - 0960-9822
VL - 26
SP - 1091
EP - 1097
JO - Current Biology
JF - Current Biology
IS - 8
ER -